abstract
Healthy aquatic ecosystems include a large diversity of organisms ranging from viruses to megavertebrates. It is our belief that there is a dynamic interplay among these myriad organisms that is essential to the health of the system. In the human medical literature the Hygiene Hypothesis has been proposed as an explanation for an observed increase in the human prevalence of various hypersensitivities such as allergies and atopy1. That hypothesis posits that individuals who mature in modern sanitized environments, particularly "Western" environments, develop innate and acquired immune experiences which result in perturbed responses when compared to more historically "natural" conditions.
We have introduced a corollary, the Aquatic Animal Hygiene Hypothesis, which may be helpful in understanding and managing the health of aquatic systems2. Our hypothesis suggests that microbes within managed aquatic systems are subject to powerful selection pressures and that the equilibrium state of managed systems is characterized by a much different microbial ecology than naturally occurring systems. This, in turn, profoundly influences the adaptive immune responses of host organisms sharing the environment. To investigate this hypothesis and establish appropriate tests of validity, we are first describing the microbial ecology of several diverse managed systems using molecular techniques and comparing these descriptions with open or natural systems. Additionally we are conducting time series analyses to evaluate stability or seasonality in these systems. Finally, we hope to test findings for correlation with health assessment data from collection animals housed in managed systems and explore the potential of manipulating the aquatic microbial milieu in ways more favorable to the optimum health and welfare of these animals3.
Modern aquaria are an excellent model system in which to study this hypothesis and explore microbial contributions to a healthy environment. Microbial communities provide important ecosystem services in natural marine systems, playing key roles in nutrient cycling and biogeochemical transformations. In artifical systems, the water quality function of microbial communities are replaced by technological approaches. Water treatment in artificial systems maintains the chemical and physical parameters of the environment within a restricted range of variation, and current management goals seek to reduce microbial abundance. Microbial ecology studies in natural systems indicate that microbial community composition and diversity responds to fluctuations in environmental variables, thus we expect that artificial environments with stable environmental parameters will have microbial communities that are less diverse and less dynamic than their natural counterparts or aquaria with more variable or open environments. We seek to determine the impact of environmental management on the microbial ecology of aquarium ecosystems, and to link observations about the diversity and dynamics of microbial communities to long-term data on animal health. We hypothesize that artificial ecosystems with lower microbial diversity may contribute to reduced immune function in aquatic mammals similar to humans in cleaner surroundings. The Shedd Aquarium and Vancouver Aquarium offer ideal means to study the Aquatic Animal Hygiene Hypothesis as it relates to marine mammals. Both aquaria regulate physical and chemical properties of their waters to some extent. However, the Vancouver Aquarium utilizes ocean water from the adjacent Burrard Inlet whereas the Shedd Aquarium uses artificial sea water. Habitats at the two aquaria provide a gradient of environmental variability in which to explore microbial diversity in marine mammal habitats. Research in microbial community ecology suggest that stability in environmental conditions affects microbial diversity and dynamics, and the Aquatic Animal Hygiene Hypothesis suggests that this may impact animal health.
Preliminary microbial community analyses suggest that microbial diversity is significantly lower in the artificial habitats compared to the natural ecosystems, thus aquarium populations of animals appear to be encountering less diverse microbial communities than their natural counterparts. In addition, microbial communities in aquaria may be more stable over time than microbial communities in the natural environment, and the stable conditions may contribute in part to decreased microbial diversity. The implication of microbial diversity as a component of a healthy environment is a promising area of research.
acknowledgements
The authors gratefully recognize the contributions of the husbandry staffs at the Shedd and Vancouver aquaria for tireless sample collection and handling and the staff of the Kent Laboratory UIUC, for equally tireless sample processing.
References
1. Martinez FD. 2001. The Coming of Age of the Hygiene Hypothesis. Respir. Res. 2:129-132.
2. Carmack TB, Van Bonn W, Poll C. 2007. Potential Implications of the Hygiene Hypothesis on Cetacean Management Systems. Abstr. Proc. IAAAM pp. 156-7.
3. Boehm JR, Chaikind B. (Eds.) 2007. Managing Cetaceans for Optimal Health: Proceedings from a workshop hosted by the John G. Shedd Aquarium, 17-18 May, Chicago, IL.